Clin J Gastroenterol (2009) 2:275–278 DOI 10.1007/s12328-009-0091-y
CASE REPORT
Advanced gastric cancer associated with nodular gastritis in a young patient Kenichiro Imai Æ Atsushi Mitsunaga Æ Tatsuo Araida Æ Shunsuke Onizawa Æ Yuurin Shin Æ Masayuki Nakano
Received: 19 March 2009 / Accepted: 10 May 2009 / Published online: 10 June 2009 Ó Springer 2009
Abstract A 20-year-old female underwent an endoscopy for epigastralgia that revealed many small, elevated nodules in the antrum that were diagnosed as nodular gastritis. The endoscopy also showed an ulcerative lesion with an uneven round wall at the greater curvature of the middle corpus. Biopsy of the ulcerative lesion yielded a diagnosis of poorly differentiated adenocarcinoma. A distal gastrectomy was performed on the basis of a diagnosis of gastric cancer associated with nodular gastritis. The intraoperative findings revealed serosal invasion of the gastric cancer and the patient tested positive for peritoneal cytology. The pathological findings revealed poorly differentiated adenocarcinoma showing invasive growth with fibrosis on the corpus and large and superficial lymphoid follicles on the miliary nodules at the antrum. The patient was positive for Helicobacter pylori infection by both the serum Helicobacter pylori antibody and histopathological findings. Keywords Nodular gastritis Gastric cancer Helicobacter pylori
K. Imai (&) T. Araida S. Onizawa Y. Shin Department of Hepato-Biliary-Pancreatic Surgery, Tokyo Women’s Medical University, Yachiyo Medical Center, 477-96 Owadashinden, Yachiyo, Chiba 276-8524, Japan e-mail: [email protected] A. Mitsunaga Department of Endoscopy, Tokyo Women’s Medical University, Yachiyo Medical Center, Chiba, Japan M. Nakano Department of Pathology, Tokyo Women’s Medical University, Yachiyo Medical Center, Chiba, Japan
Introduction Nodular gastritis is a type of gastritis that is characterized by multiple, uniform, slightly elevated lesions, called a miliary pattern, at the antrum. It may be associated with Helicobacter pylori (H. pylori) infection. In addition, gastric cancer sometimes originates from nodular gastritis. However, the clinicopathological features of patients with nodular gastritis have not been clarified. This report presents a case of a young female patient with advanced gastric cancer associated with nodular gastritis.
Case report A 20-year-old female underwent an endoscopy for epigastralgia. Endoscopy showed an ulcerative lesion at the greater curvature of the corpus. She had no family history or past medical history of illness. The laboratory results at hospital admission revealed no abnormalities including tumor markers, CEA and CA19-9. She tested positive for the serum H. pylori antibody. A barium meal test revealed an ulcerative lesion at the middle corpus (Fig. 1). Endoscopy revealed an uneven ulcerative lesion with fold convergence at the greater curvature of the corpus (Fig. 2). A biopsy yielded a diagnosis of poorly differentiated adenocarcinoma. Endoscopy also revealed unusual, slightly elevated lesions in a miliary pattern at the antrum (Fig. 3). Therefore, the patient was diagnosed with gastric cancer associated with nodular gastritis. Endoscopic ultrasonography revealed thickening of the propriomuscular layer and serosal invasion. Abdominal computed tomography (CT) showed swollen lymph nodes along the greater curvature of the stomach. A laparotomy was performed in October 2008, based on a diagnosis of advanced gastric cancer.
123
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Clin J Gastroenterol (2009) 2:275–278
Fig. 4 Pathological findings revealed poorly differentiated adenocarcinoma
Fig. 1 Barium meal showed an ulcerative lesion with a round wall at the corpus of the stomach
Fig. 5 Increased lymphoid follicles with a germinal center were seen at the antrum
Fig. 2 Endoscopy revealed an ulcerative lesion with an irregular round wall at the greater curvature of the corpus
The intraoperative findings revealed gastric cancer at the corpus with serosal invasion and no disseminated mass, but there was positive peritoneal cytology. She underwent distal gastrectomy with D2 lymph nodes dissection. The pathological findings revealed poorly differentiated adenocarcinoma showing invasive growth with fibrosis on the corpus (Fig. 4). There were large and superficial lymphoid follicles on the miliary nodules at the antrum (Fig. 5) and a metastatic lymph node along the greater curvature. The patient’s postoperative course was uneventful and she was discharged 11 days after surgery. She is undergoing chemotherapy on an outpatient basis without recurrence at 5 months after surgery.
Discussion
Fig. 3 Endoscopy showed an unusual miliary pattern of the antrum
123
Nodular gastritis is a type of gastritis that is characterized by nodular lesions in a miliary pattern at the antrum observed on endoscopy. Nodular gastritis occurs predominantly in young patients. Miyamoto et al. [1] reported that
Clin J Gastroenterol (2009) 2:275–278
0.19% of adults ages 16 years old or older who underwent endoscopy were diagnosed with nodular gastritis. Most were young and had clinical symptoms such as abdominal pain. Fujimura et al. [2] reported that the number of patients having abdominal symptoms with nodular gastritis was greater than those without nodular gastritis. Nodular gastritis is strongly associated with H. pylori infection, and the pathological findings revealed an intense inflammatory cell infiltrate consisting primarily of monocytes and an increased number of lymphoid follicles with a germinal center [3]. There is a strong possibility that nodular gastritis is associated with undifferentiated gastric cancer at the corpus [4]. This is based on findings from 39 previous reports based on a PubMed search using the key words ‘‘nodular gastritis’’ and ‘‘gastric cancer’’ for articles published between 1966 and 2008, and ‘‘Torihada-ien’’ and ‘‘Igan’’ in the Igakuchuo Zasshi for published article in Japanese between 1983 and 2008 (Table 1) [4–19]. The mean age of the patients was 34.1 years. Of the 39 patients, 30 were women. Thirty-three of the tumors were located at the corpus and 6 at the angle of the stomach. Almost all, except 1 patient, showed only poorly differentiated or undifferentiated adenocarcinoma including signet ring cell carcinoma. All patients who were tested for H. pylori infection were positive. The young woman in the current case with H. pylori infection underwent endoscopy for abdominal pain and the diffuse-type advanced gastric cancer was detected. Her clinical course was consistent with the previous cases. The characteristic findings of nodular gastritis on endoscopy were seen at the antrum; however, the histological inflammatory changes reached the corpus. Pangastritis, defined as gastritis with extreme mucosal inflammation of the entire stomach, is a risk factor for diffuse-type gastric cancer, and nodular gastritis may be a risk factor for pangastritis [20, 21]. Endoscopy for patients with nodular gastritis should be performed carefully because gastric cancer occurs at the corpus and not at the antrum, where the miliary pattern is observed. Eradication of the H. pylori infection improves endoscopic and histological findings in patients with nodular gastritis [22]. Eradication of the H. pylori infection might also prevent gastric cancer associated with nodular gastritis [23]. Atrophic gastritis, which is caused by H. pylori infection, is associated with CagA and is the risk factor for intestinal type gastric cancer. On the other hand, nodular gastritis and enlarged fold gastritis are also caused by H. pylori infection and are risk factors of diffuse-type gastric cancer. Cytokines or growth factors in the mucosa might increase the mutagenicity of gastric juice, and oxidative DNA damage, and thus increase the risk of gastric cancer in patients with
277 Table 1 Clinicopathological features of patients with gastric cancer associated with nodular gastritis Number
39
Age (years) Mean (range)
34.1 (17-69)
Gender Male
9
Female
30
Symptom Abdominal pain
7
Bleeding
3
Nausea, vomiting
2
Body weight loss Asymptomatic
1 5
Unknown
21
Location Corpus
33
Angle
6
Differentiation (type) Signet ring cell carcinoma
18
Poorly differentiated adenocarcinoma
13
Undifferentiated adenocarcinoma
2
Well-differentiated adenocarcinoma
1
(Diffuse type)
5
Stage Early
21
Advanced
18
Helicobacter pylori infection Positive Negative
30 0
Unknown
9
enlarged fold gastritis [24, 25]. However, the mechanism for the development of diffuse-type gastric cancer in patients with nodular gastritis has not yet been clarified. The risk of gastric cancer may, therefore, be caused by patient factors rather than environmental factors in patients with gastric cancer associated with nodular gastritis. Most of these patients are young and only likely to have been in the same environment for a short period of time.
References 1. Miyamoto M, Haruma K, Yoshihara M, Hiyama T, Sumioka M, Nishisaka T, et al. Nodular gastritis in adults is caused by Helicobacter pylori infection. Dig Dis Sci. 2003;48:968–75. 2. Fujimura N, Kamada T, Haruma K. Endoscopic gastritis and symptoms. Gastroenterology. 2007;44:582–6. 3. De Giacomo C, Fiaccca R, Villani L, Lisato L, Diegoli N, Donaadini A, et al. Helicobacter pylori infection and chronic gastritis: clinical, serological, and histologic correlations in children
123
278
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
Clin J Gastroenterol (2009) 2:275–278 treated with amoxicillin and colloidal bismuth subcitrate. J Pediatr Gastroenterol Nutr. 1990;111:310–6. Miyamoto M, Haruma K, Yoshihara M, Sumioka M, Nishisaka T, Tanaka S, et al. Five cases of nodular gastritis and gastric cancer: a possible association between nodular gastritis and gastric cancer. Dig Liver Dis. 2002;34:819–20. Kamada T, Haruma K, Sugiu K, Nagashima Y, Qian DM, Koga H, et al. Case of early gastric cancer with nodular gastritis. Dig Endosc. 2004;16:39–43. Tanimura T, Hashimoto T, Ono M, Suetsugu H, Kondo K, Ota M, et al. A case of juvenile gastric cancer with nodular gastritis. Koritsu Unnan Sougou Byouin Igaku Zasshi. 2006;12:11–6. (in Japanese with English abstract). Inoue K, Kanemasa H, Inoue K, Matsuimoto M, Maki K, Kajita Y, et al. A case of advanced gastric cancer with nodular gastritis in a young adult. Gastroenterol Endosc. 2007;49:185–9. (in Japanese with English abstract). Tanabe J, Kawai N, Abe T. The suppression of development to the gastric cancer by eradication for Helicobacter pylori. J Jpn Soc Gastroenterol. 2006;103:127. (in Japanese). Kitamura S, Yasuda M, Aoki R, Sokabe M, Hayashi T, Yamanoi A, et al. A case of scirrhous type gastric cancer related Epstein Barr virus infection associated with nodular gastritis. J Jpn Soc Gastroenterol. 2008;105:775. (in Japanese). Muranaka A, Kamada T, Miyamoto M, Itou K, Toudou Y, Masuyama H, et al. Clinicopathological features of 19 patients with gastric cancer associated with nodular gastritis. Gastroenterol Endosc. 2004;46(2):1924. (in Japanese). Nagashima Y, Haruma K, Kamada T, Hiramoto H, Itou T, Furuta T, et al. A case of teens with gastric cancer associated with nodular gastritis after endoscopic mucosal resection. Gastroenterol Endosc. 2004;46(1):660. (in Japanese). Kitamura S, Yasuda M, Torisu T. A case of gastric cancer associated with nodular gastritis. J Gastroenterol Cancer Screen. 2007;45:526–9. (in Japanese). Hosoi A, Uno A, Kobayashi S, Oonishi M, Nishiyama R, Akai Y, et al. A case of undifferentiated type gastric cancer associated with nodular gastritis. Prog Dig Endosc. 2006;69:62–3. (in Japanese). Nishikawa I, Tomechi T, Mori Y, Ibata Y, Matsunaka H, Higashi K, et al. A case of undifferentiated type tiny gastric cancer associated with nodular gastritis. Gastroenterol Endosc. 2008;50(2):2318. Kitamura S, Yasuda M, Torisu T, Yamanoi A, Hayashi T, Bandou G, et al. A case of gastric cancer associated with nodular
123
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
gastritis which was detected on upper gastrointestinal study during annual health examination. J Gastroenterol Cancer Screen. 2006;44:424. (in Japanese). Ogiyama S, Joudou F, Iishi H, Yamada T, Higashino A, Sugimoto N, et al. A case of juvenile gastric cancer with nodular gastritis. J Jpn Soc Intern Med. 2005;94:168. (in Japanese). Abe H, Uno A, Yokota T, Yamada K, Itou K, Oyama K, et al. A case of juvenile advanced gastric cancer detected on hematemesis. Prog Dig Endosc. 2008;74:78. (in Japanese). Ohira M, Ueda H, Furuta R, Kiki J, Mizuta H, Miyamoto K, et al. A case of small gastric cancer associated with nodular gastritis in 21-year-old patient. Gastroenterol Endosc. 2005;47(1):828. Yamashita S, Hirao M, Fujitani K, Ishihi M, Masuda S, Kashiwazaki M, et al. A case of advanced gastric cancer associated with nodular gastritis. J Jpn Soc Gastroenterol. 2006;103:290. (in Japanese). Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter infection and development of gastric cancer. N Eng J Med. 2001;345:754–89. (in Japanese). Sakaguchi M, Amemoto K, Honda M, Hashimoto T, Asakuma Y, Shimada M, et al. Clinical evaluation of nodular gastritis; followup by endoscopy and histopathology. Gastroenterology. 2006;48:2477–85. (in Japanese with English abstract). IARC Working Group on the elevation of carcinogenic risks to humans. Helicobacter pylori. Schistosomes, liver flukes and Helicobacter pylori: views and expert opinions of IARC Working Group on elevation of carcinogenic risks to humans. Lyon: IARC; 1994. p. 177–240. Correa P, Fontham ET, Bravo JC, Bravo LE, Ruiz B, Zarama G, et al. Chemoprevention of gastric dysplasia: randomized trial of antioxidant supplements and anti-helicobacter pylori therapy. J Natl Cancer Inst. 2000;92:1881–8. Nishibayashi H, Kanayama S, Kiyohara T, Yamamoto K, Miyazaki Y, Yasunaga Y, et al. Helicobacter pylori-induced enlarged-fold gastritis is associated with increased mutagenicity of gastric juice, increased oxidative DNA damage, and an increased risk of gastric carcinoma. J Gastroenterol Hepatol. 2003;18:1384–91. Yasunaga Y, Shinomura Y, Kanayama S, Higashimoto Y, Yabu M, Miyazaki Y, et al. Increased production of interleukin 1 beta and hepatocyte growth factor may contribute to foveolar hyperplasia in enlarged fold gastritis. Gut. 1996;39:787–94.
CASE REPORT
Advanced gastric cancer associated with nodular gastritis in a young patient Kenichiro Imai Æ Atsushi Mitsunaga Æ Tatsuo Araida Æ Shunsuke Onizawa Æ Yuurin Shin Æ Masayuki Nakano
Received: 19 March 2009 / Accepted: 10 May 2009 / Published online: 10 June 2009 Ó Springer 2009
Abstract A 20-year-old female underwent an endoscopy for epigastralgia that revealed many small, elevated nodules in the antrum that were diagnosed as nodular gastritis. The endoscopy also showed an ulcerative lesion with an uneven round wall at the greater curvature of the middle corpus. Biopsy of the ulcerative lesion yielded a diagnosis of poorly differentiated adenocarcinoma. A distal gastrectomy was performed on the basis of a diagnosis of gastric cancer associated with nodular gastritis. The intraoperative findings revealed serosal invasion of the gastric cancer and the patient tested positive for peritoneal cytology. The pathological findings revealed poorly differentiated adenocarcinoma showing invasive growth with fibrosis on the corpus and large and superficial lymphoid follicles on the miliary nodules at the antrum. The patient was positive for Helicobacter pylori infection by both the serum Helicobacter pylori antibody and histopathological findings. Keywords Nodular gastritis Gastric cancer Helicobacter pylori
K. Imai (&) T. Araida S. Onizawa Y. Shin Department of Hepato-Biliary-Pancreatic Surgery, Tokyo Women’s Medical University, Yachiyo Medical Center, 477-96 Owadashinden, Yachiyo, Chiba 276-8524, Japan e-mail: [email protected] A. Mitsunaga Department of Endoscopy, Tokyo Women’s Medical University, Yachiyo Medical Center, Chiba, Japan M. Nakano Department of Pathology, Tokyo Women’s Medical University, Yachiyo Medical Center, Chiba, Japan
Introduction Nodular gastritis is a type of gastritis that is characterized by multiple, uniform, slightly elevated lesions, called a miliary pattern, at the antrum. It may be associated with Helicobacter pylori (H. pylori) infection. In addition, gastric cancer sometimes originates from nodular gastritis. However, the clinicopathological features of patients with nodular gastritis have not been clarified. This report presents a case of a young female patient with advanced gastric cancer associated with nodular gastritis.
Case report A 20-year-old female underwent an endoscopy for epigastralgia. Endoscopy showed an ulcerative lesion at the greater curvature of the corpus. She had no family history or past medical history of illness. The laboratory results at hospital admission revealed no abnormalities including tumor markers, CEA and CA19-9. She tested positive for the serum H. pylori antibody. A barium meal test revealed an ulcerative lesion at the middle corpus (Fig. 1). Endoscopy revealed an uneven ulcerative lesion with fold convergence at the greater curvature of the corpus (Fig. 2). A biopsy yielded a diagnosis of poorly differentiated adenocarcinoma. Endoscopy also revealed unusual, slightly elevated lesions in a miliary pattern at the antrum (Fig. 3). Therefore, the patient was diagnosed with gastric cancer associated with nodular gastritis. Endoscopic ultrasonography revealed thickening of the propriomuscular layer and serosal invasion. Abdominal computed tomography (CT) showed swollen lymph nodes along the greater curvature of the stomach. A laparotomy was performed in October 2008, based on a diagnosis of advanced gastric cancer.
123
276
Clin J Gastroenterol (2009) 2:275–278
Fig. 4 Pathological findings revealed poorly differentiated adenocarcinoma
Fig. 1 Barium meal showed an ulcerative lesion with a round wall at the corpus of the stomach
Fig. 5 Increased lymphoid follicles with a germinal center were seen at the antrum
Fig. 2 Endoscopy revealed an ulcerative lesion with an irregular round wall at the greater curvature of the corpus
The intraoperative findings revealed gastric cancer at the corpus with serosal invasion and no disseminated mass, but there was positive peritoneal cytology. She underwent distal gastrectomy with D2 lymph nodes dissection. The pathological findings revealed poorly differentiated adenocarcinoma showing invasive growth with fibrosis on the corpus (Fig. 4). There were large and superficial lymphoid follicles on the miliary nodules at the antrum (Fig. 5) and a metastatic lymph node along the greater curvature. The patient’s postoperative course was uneventful and she was discharged 11 days after surgery. She is undergoing chemotherapy on an outpatient basis without recurrence at 5 months after surgery.
Discussion
Fig. 3 Endoscopy showed an unusual miliary pattern of the antrum
123
Nodular gastritis is a type of gastritis that is characterized by nodular lesions in a miliary pattern at the antrum observed on endoscopy. Nodular gastritis occurs predominantly in young patients. Miyamoto et al. [1] reported that
Clin J Gastroenterol (2009) 2:275–278
0.19% of adults ages 16 years old or older who underwent endoscopy were diagnosed with nodular gastritis. Most were young and had clinical symptoms such as abdominal pain. Fujimura et al. [2] reported that the number of patients having abdominal symptoms with nodular gastritis was greater than those without nodular gastritis. Nodular gastritis is strongly associated with H. pylori infection, and the pathological findings revealed an intense inflammatory cell infiltrate consisting primarily of monocytes and an increased number of lymphoid follicles with a germinal center [3]. There is a strong possibility that nodular gastritis is associated with undifferentiated gastric cancer at the corpus [4]. This is based on findings from 39 previous reports based on a PubMed search using the key words ‘‘nodular gastritis’’ and ‘‘gastric cancer’’ for articles published between 1966 and 2008, and ‘‘Torihada-ien’’ and ‘‘Igan’’ in the Igakuchuo Zasshi for published article in Japanese between 1983 and 2008 (Table 1) [4–19]. The mean age of the patients was 34.1 years. Of the 39 patients, 30 were women. Thirty-three of the tumors were located at the corpus and 6 at the angle of the stomach. Almost all, except 1 patient, showed only poorly differentiated or undifferentiated adenocarcinoma including signet ring cell carcinoma. All patients who were tested for H. pylori infection were positive. The young woman in the current case with H. pylori infection underwent endoscopy for abdominal pain and the diffuse-type advanced gastric cancer was detected. Her clinical course was consistent with the previous cases. The characteristic findings of nodular gastritis on endoscopy were seen at the antrum; however, the histological inflammatory changes reached the corpus. Pangastritis, defined as gastritis with extreme mucosal inflammation of the entire stomach, is a risk factor for diffuse-type gastric cancer, and nodular gastritis may be a risk factor for pangastritis [20, 21]. Endoscopy for patients with nodular gastritis should be performed carefully because gastric cancer occurs at the corpus and not at the antrum, where the miliary pattern is observed. Eradication of the H. pylori infection improves endoscopic and histological findings in patients with nodular gastritis [22]. Eradication of the H. pylori infection might also prevent gastric cancer associated with nodular gastritis [23]. Atrophic gastritis, which is caused by H. pylori infection, is associated with CagA and is the risk factor for intestinal type gastric cancer. On the other hand, nodular gastritis and enlarged fold gastritis are also caused by H. pylori infection and are risk factors of diffuse-type gastric cancer. Cytokines or growth factors in the mucosa might increase the mutagenicity of gastric juice, and oxidative DNA damage, and thus increase the risk of gastric cancer in patients with
277 Table 1 Clinicopathological features of patients with gastric cancer associated with nodular gastritis Number
39
Age (years) Mean (range)
34.1 (17-69)
Gender Male
9
Female
30
Symptom Abdominal pain
7
Bleeding
3
Nausea, vomiting
2
Body weight loss Asymptomatic
1 5
Unknown
21
Location Corpus
33
Angle
6
Differentiation (type) Signet ring cell carcinoma
18
Poorly differentiated adenocarcinoma
13
Undifferentiated adenocarcinoma
2
Well-differentiated adenocarcinoma
1
(Diffuse type)
5
Stage Early
21
Advanced
18
Helicobacter pylori infection Positive Negative
30 0
Unknown
9
enlarged fold gastritis [24, 25]. However, the mechanism for the development of diffuse-type gastric cancer in patients with nodular gastritis has not yet been clarified. The risk of gastric cancer may, therefore, be caused by patient factors rather than environmental factors in patients with gastric cancer associated with nodular gastritis. Most of these patients are young and only likely to have been in the same environment for a short period of time.
References 1. Miyamoto M, Haruma K, Yoshihara M, Hiyama T, Sumioka M, Nishisaka T, et al. Nodular gastritis in adults is caused by Helicobacter pylori infection. Dig Dis Sci. 2003;48:968–75. 2. Fujimura N, Kamada T, Haruma K. Endoscopic gastritis and symptoms. Gastroenterology. 2007;44:582–6. 3. De Giacomo C, Fiaccca R, Villani L, Lisato L, Diegoli N, Donaadini A, et al. Helicobacter pylori infection and chronic gastritis: clinical, serological, and histologic correlations in children
123
278
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
Clin J Gastroenterol (2009) 2:275–278 treated with amoxicillin and colloidal bismuth subcitrate. J Pediatr Gastroenterol Nutr. 1990;111:310–6. Miyamoto M, Haruma K, Yoshihara M, Sumioka M, Nishisaka T, Tanaka S, et al. Five cases of nodular gastritis and gastric cancer: a possible association between nodular gastritis and gastric cancer. Dig Liver Dis. 2002;34:819–20. Kamada T, Haruma K, Sugiu K, Nagashima Y, Qian DM, Koga H, et al. Case of early gastric cancer with nodular gastritis. Dig Endosc. 2004;16:39–43. Tanimura T, Hashimoto T, Ono M, Suetsugu H, Kondo K, Ota M, et al. A case of juvenile gastric cancer with nodular gastritis. Koritsu Unnan Sougou Byouin Igaku Zasshi. 2006;12:11–6. (in Japanese with English abstract). Inoue K, Kanemasa H, Inoue K, Matsuimoto M, Maki K, Kajita Y, et al. A case of advanced gastric cancer with nodular gastritis in a young adult. Gastroenterol Endosc. 2007;49:185–9. (in Japanese with English abstract). Tanabe J, Kawai N, Abe T. The suppression of development to the gastric cancer by eradication for Helicobacter pylori. J Jpn Soc Gastroenterol. 2006;103:127. (in Japanese). Kitamura S, Yasuda M, Aoki R, Sokabe M, Hayashi T, Yamanoi A, et al. A case of scirrhous type gastric cancer related Epstein Barr virus infection associated with nodular gastritis. J Jpn Soc Gastroenterol. 2008;105:775. (in Japanese). Muranaka A, Kamada T, Miyamoto M, Itou K, Toudou Y, Masuyama H, et al. Clinicopathological features of 19 patients with gastric cancer associated with nodular gastritis. Gastroenterol Endosc. 2004;46(2):1924. (in Japanese). Nagashima Y, Haruma K, Kamada T, Hiramoto H, Itou T, Furuta T, et al. A case of teens with gastric cancer associated with nodular gastritis after endoscopic mucosal resection. Gastroenterol Endosc. 2004;46(1):660. (in Japanese). Kitamura S, Yasuda M, Torisu T. A case of gastric cancer associated with nodular gastritis. J Gastroenterol Cancer Screen. 2007;45:526–9. (in Japanese). Hosoi A, Uno A, Kobayashi S, Oonishi M, Nishiyama R, Akai Y, et al. A case of undifferentiated type gastric cancer associated with nodular gastritis. Prog Dig Endosc. 2006;69:62–3. (in Japanese). Nishikawa I, Tomechi T, Mori Y, Ibata Y, Matsunaka H, Higashi K, et al. A case of undifferentiated type tiny gastric cancer associated with nodular gastritis. Gastroenterol Endosc. 2008;50(2):2318. Kitamura S, Yasuda M, Torisu T, Yamanoi A, Hayashi T, Bandou G, et al. A case of gastric cancer associated with nodular
123
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
gastritis which was detected on upper gastrointestinal study during annual health examination. J Gastroenterol Cancer Screen. 2006;44:424. (in Japanese). Ogiyama S, Joudou F, Iishi H, Yamada T, Higashino A, Sugimoto N, et al. A case of juvenile gastric cancer with nodular gastritis. J Jpn Soc Intern Med. 2005;94:168. (in Japanese). Abe H, Uno A, Yokota T, Yamada K, Itou K, Oyama K, et al. A case of juvenile advanced gastric cancer detected on hematemesis. Prog Dig Endosc. 2008;74:78. (in Japanese). Ohira M, Ueda H, Furuta R, Kiki J, Mizuta H, Miyamoto K, et al. A case of small gastric cancer associated with nodular gastritis in 21-year-old patient. Gastroenterol Endosc. 2005;47(1):828. Yamashita S, Hirao M, Fujitani K, Ishihi M, Masuda S, Kashiwazaki M, et al. A case of advanced gastric cancer associated with nodular gastritis. J Jpn Soc Gastroenterol. 2006;103:290. (in Japanese). Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter infection and development of gastric cancer. N Eng J Med. 2001;345:754–89. (in Japanese). Sakaguchi M, Amemoto K, Honda M, Hashimoto T, Asakuma Y, Shimada M, et al. Clinical evaluation of nodular gastritis; followup by endoscopy and histopathology. Gastroenterology. 2006;48:2477–85. (in Japanese with English abstract). IARC Working Group on the elevation of carcinogenic risks to humans. Helicobacter pylori. Schistosomes, liver flukes and Helicobacter pylori: views and expert opinions of IARC Working Group on elevation of carcinogenic risks to humans. Lyon: IARC; 1994. p. 177–240. Correa P, Fontham ET, Bravo JC, Bravo LE, Ruiz B, Zarama G, et al. Chemoprevention of gastric dysplasia: randomized trial of antioxidant supplements and anti-helicobacter pylori therapy. J Natl Cancer Inst. 2000;92:1881–8. Nishibayashi H, Kanayama S, Kiyohara T, Yamamoto K, Miyazaki Y, Yasunaga Y, et al. Helicobacter pylori-induced enlarged-fold gastritis is associated with increased mutagenicity of gastric juice, increased oxidative DNA damage, and an increased risk of gastric carcinoma. J Gastroenterol Hepatol. 2003;18:1384–91. Yasunaga Y, Shinomura Y, Kanayama S, Higashimoto Y, Yabu M, Miyazaki Y, et al. Increased production of interleukin 1 beta and hepatocyte growth factor may contribute to foveolar hyperplasia in enlarged fold gastritis. Gut. 1996;39:787–94.
